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The Opera di Santa Maria del Fiore was founded by the Florentine Republic in 1296 with the participation of the city's ecclesiastical authorities to oversee construction of the new cathedral and its bell tower.

Once the church was consecrated on 25 March 1436 and its architectural structure was complete, the Opera's primary task became the conservation and embellishment of this complex of monuments. The baptistry of San Giovanni came under its jurisdiction in 1777 and the Museo dell'Opera di Santa Maria del Fiore, set up to house works of art which had been removed from the cathedral and baptistry over the centuries, joined it in 1891.

Today the Opera, in its capacity as a "fabbriceria", is subject to the Concordat Laws of 1929 and 1984. It is run by a Board of Directors comprising seven members appointed by Interior Ministry decree with a three-year mandate, who elect one of their number to the post of chairman.

In 1998 the Opera was legally recognised as not-for-profit organisation pursuing, as part of its institutional aims, the protection, promotion and enhancement of the religious, civic, cultural and historical functions of the monuments in its care.